TRABAJOS DE PREHISTORIA

49, 1992, pp. 51-68

HETEROCHRONY AND THE PALEOANTHROPOLOGICAL RECORD: THE ORIGINS

OF THE GENUS HOMO RECONSIDERED

BY

JOS E MARIA BERMUDEZ DE CASTRO n

MANUEL DOMINGUEZ-RODRIGO rO) (sequence of authorship alphabetical)

ABSTRACT In this paper a critical review is made of the main theories concerning the process of
appearance and subsequent evolutionary success of the genus Horno. Furthennore,
the current evidence coming from the paleoanthropological record is analyzed in
arder to establish the interrelation between the biological and cultural factors impli-
cated in that process. It is suggested that the evidence of the paleoanthropological
record presumably related to early Horno is basically explicable from the consideration
of the strengthening of the social links in the bosom of the group, likely due to the
abandonment of an hierarchyzed society in favour of a more cooperative one. This
change does not necessarily imply, nor does it exclude the possibility of the formation
of stable nuclear families, and probably appeared as a result of a biological change
consisting of a decrease of the rate of development, that produced certain prolongation
of all life history periods, and sorne delay in the offset signal for growth (but resulting
in paedomorphic adults). As a consequence, there was an increase of the interactive
and operative capacities that permitted the emergence of a novel and successful
ecological niche under the new environmental conditions arised in the late Pliocene.
Other additional heterochrony processes are suggested to explain the subsequent
morphological evolution of the genus Horno.

RESUMEN En este trabajo se realiza una revisión critica de las principales teorias relacionadas'
con el proceso de aparición y subsiguiente éxito evolutivo del género Horno. Se
analiza asimismo la evidencia más reciente procedente del registro paleoantropológico,
para establecer la interrelación entre los factores biológicos y culturales implicados
en dicho proceso. Se sugiere que la evidencia del registro paleoantropológico presu-
miblemente relacionado con los primeros representantes del género Horno puede
explicarse básicamente desde la consideración de un reforzamiento de los lazos
sociales en el seno del grupo, relacionado con el abandono de una sociedad jerárquica
hacia una sociedad cooperativa. Este cambio no implica necesariamente, pero tampoco
excluye la posibilidad de formación de núcleos familiares estables, y probablemente
surgió como resultado de un cambio biológico consistente en una disminución de la

n Colaborador Científico.
('> Museo Nacional de Ciencias Naturales. Madrid.

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tasa de desalTollo, que produjo una cierta prolongación de los periodos de crecimiento
y cierto retraso del momento final del crecimiento (pero resultando en adultos paedo-
mórficos). Como consecuencia de este proceso, se produjo un incremento de las
capacidades interactiva y operativa, que pcnnitió la emergencia de un nicho ecológico
novedoso y eficaz para las nuevas condiciones medioambientales surgidas al final del
Plioceno. Se sugieren otros procesos de heterocronía adicionales para cxplicar cambios
morfológicos posteriores en el géncro Homo.

Key worda Hominidos. Modelos de evolución. Heterocronia.

Palabras clave Hominids. Evolutionary models. Heterochrony.

"I{ early 11Om;nids were growing like humans lhen

why weren'! lhey humans?"
Bromage (1986: 310)

INTRODUCTION

Traditionally, the models that have been proposed to explain human evolution were conceived
considering both the significance of the biological processes supposedly implicated, and the interaction
of these with what we have named culture in its broadest sense. Cultural factors, however, have
been principally used in those models which have searched for an explanation for particular
qualitative and quantitative changes observed through the fossil record in the species of the genus
Horno (Brace, 1962; Dahlberg, 1963; Wolpoff, 1979; Smith, 1983). Sorne authors (Bol k, 1926; de Beer,
1948; Keith, 1949; Montagu, 1962; Gould, 1977) have elaborated general models conceming human
evolution in order to interpret the remarkable morphological differences that separate Horno
sapiens from an ancestor that tends to be identified with chimpanzees and gorillas, our nearest
living relatives. It is not hardly surprising that in these models the arguments coming from the
observation of the fossil record had a slight relevance. The fossil record obtained up to the late
sixties was in fact very limited, and this circumstance lent itself easily to erroneous interpretations.
However, the findings of the two last decades, specially those of Hadar, Ethiopia (Johanson el al,
1982), Laetoli, Tanzania (Johanson & White, 1979), Koobi Fora, Kenya (Leakey & Wood, 1973, 1974;
Day & Leakey, 1973; Day el al, 1976; Leakey & Walker, 1985; Brown el al, 1985; Leakey & Walker,
1988), and Swartkrans, South Africa (Grine, 1989) have permitted to reach a better knowledge of
the first stages of hominid evolution, not without, of course, numerous question marks and inter-
pretations, which in a future will also be probably considered as erroneous. Notwithstanding ~hat, a
recent revision of the issue of neoteny in human evolution (Shea, 1989) does not inelude available
information coming from the fossil record evidence.
On the other hand, new methods and specially an impresive set of new technologies are being
applied to the study of this evidence. Therefore, no research trying to test models of human
evolution can be unaware of the data that are potentially offered by the hominid fossil record. In
this regard, Bromage (1986, 1987) has tested for the first time the model of human evolution
generally accepted (Gould, 1977) exclusively by means of the study of hominid fossils, and has
presented an altemative model capable of being also corroborated by the fossil record evidence.
But, besides human fossils, the sedimentary rocks preserve a precise information on the sorne of
the activities of early hominids. This information has been used to propose sorne models of hominid
behaviour (Binford, 1981; Isaac, 1983; Potts, 1984), and to approach the ecological ni che of the first
representants of the genus Horno (Potts, 1988). At present, the elaboration of models conceming
human evolution ought to be approached from a broad perspective, using different sources of
knowledge mainly Archaeology, Biology of Development, Genetics, Ecology and Palaeontology. Our

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aim here is to make a critical revision of previous models on human evolution, and to use most of
the available information to obtain a more comprehensive view uf the evolution of our genus. The
study in detail of the evolution of other hominid groups (e.g. Paral1lhropus) is outside the limits of
the present paper. However, we will make sorne references to these groups beca use, we believe,
they are of paramount importance to understand the evolutionary history of the genus Horno.

BIOLOGICAL BASIS FOR A MODEL OF HUMAN EVOLUTION

The similarities among the infantile individuals of orang-outang, chimpanzee and gorilla and the
adults of our own species were not ignored by the scientists of the 19th century (see Gould, 1977).
This kind of observations led the dutch anatomist Louis Bolk to elaborate his «Fetalization Theory»
throughout several works published in the twenties. According to Bolk (1926), human evolution was
characterized by a physiological retardation of development, probably produced by a simple alteration
of the endocrine system, that caused the somatic retention of the juvenile proportions present in
our ancestors. This claim was strongly rejected and, we believe, unfairly ridiculed beca use it was
not in harmony with the prevailing evolutionary paradigm.
Gould (1977) considers the problem of human evolution from the perspective of the causal
relations existing between the modification of the ontogenetic development and the evolutionary
changes that separate Horno sapiens from an ancestor, probably very similar to the living anthropoids.
Thus, Gould retrieves Bolk's Fetalization Theory, rejecting those aspects incompatible with the valid
evolutionary paradigm, and introducing other elements which give a new support to Bolk's insight.
Continuing with a previous tradition, Gould (1977) used a considerable and diverse amount of
morphological distintions between living humans and other primates as the source of data to
elaborate his model of human evolution. In the chapter ten of his book, he only occasionally used
the fossil record evidence to corroborate his conclusions.
Gould (1977) considers that we are essentially neotenous, not only because a careful study of
our species allows us to elaborate a list of basic paedomorphic features, but because cc ••• a general
temporal retardation of development has clearly characterized human evolution. This retardation
established a matrix within which all trends in the evolution of human morphology must be
assesed» (p. 363). However, not onIy did he agree with the aeceptance that Horno sapiens is the
result of a process of neoteny, but he was also encouraged to search for an adaptive significance
for the retardation of development in our species. Firstly, he points out that the early stages of
ontogeny preserve a great potentiality for news adaptations. Moreover, he thinks that hominids
were engaged in a general tendency to increasing size and, as a consequence, to reach an extreme
specialization, and, therefore, he claims that cc •••retardation provided the only "escape" from an
ancestral allometry and the only path to a favored adaptatioo» (Gould, 1977: 397).
The delay in the growth periods is really a common characteristic in the evolution of primates
(see Schultz, 1956). This feature, according to Gould (1977), was notably apparent in human
evolution through an extended childhood and a delayed sexual maturation. This delay operated
sinergistically with other key aspects of the hominization process: upright posture, intelligence, and
socialization. The increase of the endocranial capacity, with the resulting increase of the intelligence,
was achieved by means of a prolongation of the fetal growth trends; whereas an extended childhood
faeilitates the obtaining of a greater grade of knowledge, and favours the strenghthening of family
links through the consequent and necessary cares required by the offspring (Gould, 1977).

THE FOSSIL RECORD EVIDENCE

The hominid fossil record would seem to confirm Gould's model to understand human evolution,
sine e the upright posture and a slight increase of endocranial capacity in relation to the great apes

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characterize the species of Australopithecus. Moreover, Mann's (1975) original sludy on the dental
development pattems and the skeletal maturation of South African early hominids indicated that
australopithecines were characterized by a long childhood dependency periodo
The fossil hominids recovered in Hadar (Ethiopia) and Laetoli (Tanzania) in the seventies were a
revulsive for theories about human evolution, on demonstrating that there was not a causal and
reciprocal relationship between the erect posture and the increase in brain size that characterize the
evolution of the gen us Horno. During more than t wo million years certain hominids had an erect
posture without showing a significant relative increase of their brain sizes. The encephalization
quotients (EQ = the ratio of the observed brain size and the expected brain size) estimated by
Martin (1983) were very similar in A. afarensis and A. africanus and, though the respective EQ
estimated by this author for Paranllzropus robustus and P. boisei were greater than those of
Auslralopilhecus, these quotients were only slightly higher than the EQ estimated for chimpanzees.
The significant increase of the EQ in hominids occurs for the first time with the appearance of the
genus Horno. Martin (1983) calculates that the EQ for H habilis was a 8096 higher than that of A.
afarensis.
On the other hand, Bromage & Dean (1985) estimated the age at death of specimens belonging
to A. afarensis, A. africanus, P. robustus and H habilis based on a scanning electron microscopy
(SEM) study of surface manifestations of incremental growth lines in enamel (perikymata). These
authors conclude that Plio-Pleistocene hominids had periods of growth and development shorter
than those of modem humans, and similar to those of living great apes. Bromage & Dean's (1985)
paper has started an interesting debate among those scholars who have arrived at a similar
conclusion (Smith, 1986; Beynon & Dean, 1988; Conroy & Vannier, 1987), and those who consider
that the methods used by all these authors are not valid to conclude that Plio-Pleistocene hominids
had abbreviated growth periods relative to modem humans (Mann el al, 1987; Mann, 1988; Simpson
el al, 1990; Mann el al, 1990). Simpson el al (1990) observed, in accordance with previous papers
(Broom & Robinson, 1951; Bromage, 1986, 1987; Smith, 1986; Dean, 1987; Grine, 1987; Beynon &
Dean, 1988), that A. afarensis and A. africanus exhibited a more ape-like pattern in their dental
development sequence; whereas P. robustus and P. boisei were more human-like in relation to this
featurt;. These last species showed a unique dental development not shared either with modem
humans or with living great apes (Bromage, 1986, 1987; Smith, 1986). Simpson el al (1990),
however, consider that each early hominid group have different dental maturational and eruptive
pattems as a direct functional response to their different facial growth patterns, and that, therefore,
the pattem of dental developmental events cannot be used to establish rates of general development.
With regard to this controversy, we cannot ignore that all Australopithecus and Paranthropus
specimens examined up to date have shown enamel incremental growth and dental development
pattems that differ from those observed in modem humans, and that suggest growth and develop-
ment periods similar to those of great apes for the species of the two genera. There are a large
amount of data which have permitted to elaborate preliminary charts of development everits for
Australopithecus and Paranthropus (Aiello & Dean, 1990). Furthermore, there is a higher correlation
between dental and chronological age (Demirjian, 1978) that justifies the validity of the methods
used in these studies (Bromage & Dean, 1985; Smith, 1986). But the essential question to this debate
has been established by Bromage: «.. .if early hominids were growing like humans, then why were
they not human in such characters as brain and body size?» (Bromage, 1987: 268).
However, there are not enough data yet to elaborate a chart of development events for early
Horno (Beynon & Dean, 1985; Aiello & Dean, 1990). The SEM examination of the limited young
specimens attributed to early Horno suggests that the crowns of incisor teeth were formed more
rapidly than those of modem humans, and that the incisors and first molars emerged close together
in the growth .period like in Paranthropus and modem humans (Beynon & Dean, 1988). The only
specimen, ER-820, of early Horno that permits a confident analysis, indicates a minimum chronolo-
gical age at death that represents the 7596 of the estimated age at death using human dental
development schedules (Bromage & Dean, 1985; see also Aiello & Dean, 1990). Similar estimations

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in Australopithecus and Paranthropus indicate chrunological ages at death, which range between
51 % and 73 % of the estimated ages using human charts of devclopment (Bromage & Dean, 1985).
Therefore, though the hypothesis that early Horno had a development period shorter than that of
modem humans ought to be seriously considered, the claim that «... the trend for prolongation of
the growth period had not begun with this group" (Bromage & Dcan, 1985: 2) is still far from being
justified.
Bromage (1986) concludes that A. Afarensis, A. africanus and early Horno shared a similar
craniofacial remodeling pattem. The differences in craniofacial morphology among these species
are due, according to this author, to alterations in rates of remodeling activities. These observations
led Bromage to conclude ~~ ... that a heterogeneous set of heterochronic processes have combined to
define certain adaptive trends in hominids, thus denying the reality of the global concept of neoteny
to explain the ontogenetic sequences characterizing the course of human evolutiofl» (p. 3). Bromage
(1986, 1987) uses the weak evidence represented by the ER-820 specimen, and assumes that early
Horno shared a growth and development periods similar to that of Australopithecus. Taking into
account the partition of heterochrony between rate and time hypermorphosis considered by Shea
(1983) to explain certain size differences of the skull and body weight amongst the African apes,
Bromage (1956, 1987) concludes that the increase in the brain and body sizes from Australopithecus
to early Horno must have been due to rate hypermorphosis; Le. the changes observed between
Australopithecus and early Horno would have happened mantaining the ancestral allometric relation
and the ancestral length of ontogeny in time, but increasing the rate of the overall weight growth in
the given time. Early Homo, therefore, would be a peramorphic species in relation to Australopithecus.
The increase in body size from Australopithecus to Paranthropus was due, according to Bromage
(1986, 1987), to rate hypermorphosis as well, but on a larger scale.
In order to explain subsequent phases of human evolution, Bromage (1986, 1987) examines a
paper published by Hemmer in 1969. This author studied the interspecific allometric relationship
between the craniallength (g-op) and the face length (pr-ba). Hemmers results pointed out that the
transition Australopithecus - H. erectus was characterized by a transposition of the allometric
relationship between the two variables (fig. 3, p. 180). Therefore, this transition did not occur by
means of a simple global increase of the brain size since «••. such an enlargement would imply a
disproportionate enlargement of the facial skeleton, with compression of the braincase and formation
of strong crests by the enormously developed jaw musculature, making impossible any increase in
braincase capacity» (Hemmer, 1969: 180). According to this author, the change in the allometric
level (allometric transposition) between the cranial length and the face length from an Australopit.
hecus type like the «habilis» from Olduvai Bed n must be considered as the moment of appearance
of H. sapiens in his earliest form (Hemmer, 1969). The origin of this allometric transposition may be
found, according to Hemmer, in a change of the ontogenetic growth occurred at a certain time of
hominid evolution (Hemmer, 1967).
Bromage (1986, 1987) justifies this change by pointing out that the phylogenetic increase of the
cranial capacity runs up against the ontogenetic threshold that represents the size of the mother' ~
pelvic inlet. Bromage claims that this limit was reached at or during the H. erectus grade, and that
subsequent increases of cranial capacity were achieved by means of a fetal growth trajectory for
the brain after birth (Bromage, 1986, 1987). This author supports his conclusion in Martin's (1983)
observations on the isometric relations between primate neonate and adult brain weigths. The
empirical data led Martin (1983) to conclude that at an adult hominid cranial capacity of 850 cm3
(or at the H. erectus grade) it was necessary to extend the fetal growth trajectory of the brain into
postnatal life. In contrast to other primates, the fetal brain growth trajectory in modem humans
continues for ayear after birth (Martin, 1983). Bromage (1986, 1987) thinks that Shea's (1983)
classification of time hypermorphosis (1) fit well the pattem of development of the modem human
brain. Therefore, human evolution could be defined by a transition from a developing brain/body

(1) Time hypennorphosis would be equivalent to hyperm~rphosis in the traditional terminology (Shea, 1983).

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S6 JOSE MARIA BE;-RMUDEZ DE CASTRO Y MANUEL DOMINGUEZ-RODRIGO

relationship characterized by rate hypermorphosis to a relationship characterized by time hyper-

morphosis during H. erectus times (Bromage, 1986, 1987).
The hypermorphosis process (de Beer, 1930) has been defined as «retardation of maturation with
respect to somatic development... Ontogeny is simply prolonged because maturation has been
delayed,. (Gould, 1977: 255-256), or as «An extension of the juvenile growth period, caused by a
delay in onset of maturation,. (McNamara: 1986, 10). Alberch el al (1979) also write ((A positive
perturbation, +a~, in offset signal (for growth) also produces a peramorphic descendant by a
process of hypermorphosis" (Fig. 16, p. 305). Therefore, if we accept that the evolution of the genus
Horno was characterized by a process of hypennorphosis, we also accept that: 1) the fetal. infantile
and juvenile rates of growth and development, as well as the ancestral growth allometries, were
maintained during the course of human evolution, and 2) the differences between early Horno and
H sapiens were simply due to a prolongation of the ontogenetic trajectory (juvenile phase of
growth).
Evidently, the definition of the process of hypennorphosis and its implications do not agree with
Bromage's observations (1986). If the Plio-Pleistocene hominids had growth periods similar to those
of the living great apes, then the course of human evolution was characterized neither by an
extension of late ontogenetic development (hypermorphosis), nor by the extension of a specific
6ntogenetic period (e.g. gestation), but by sorne increase of any of the «infinite» phases (2) that we
are able to consider through human development. From an evolutionary point of view, this process
can only be explained by a decrease of the morphological development rate (neoteny), and the
subsequent increase in the time period of the different growth allometries through the overall
ontogeny. This is in accordance with the observations of Martin (1983) that the fetal allometric
growth relationship between the brain and body size continues for ayear after birth. In this respect,
we ought not to consider that the birth time denotes an important moment of our development, but
it rather responds to an obstetric necessity: the passage of an organism with a certain size across a
canal of certain dimensions.
Therefore, we believe, according to previous elaims (Montagu, 1962; Lorenz, 1971; Krogman,
1972; Gould, 1977, among others) that the hypothesis that human evolution (or the evolution of the
genus Horno) was characterized by an heterochronic process of neoteny can be still supported. The
new evidence furnished by the fossil record indicates that during two million years or more the
hominids had growth and development periods at least similar to that of living great apes. But,
when did an increase of this period in hominid evolution begin? Bromage (1986) believes that ((Rate
hypermorphosis made it possible to alter the brain/body ratios during succesive grades of hominid
evolution without requiring any alteration in the length of the growth and development periods»
(p. 333). However, a process of rate hypennorphosis implies that the ancestral allometric relation is
maintained in the descendant species (Shea, 1983). We agree with Bromage (1986, 1987) that a
change of the ancestral allometry for the body /brain size relation occurred between Australopithecus
and early Horno, but not by means of a process of rate hypennorphosis. The figure 1· is a
reproduction from Hemmer's (1969) figure 2, that ineludes data from hominids recovered subse-
quentIy to the publication of his papero The 1.7-1.9 Myr old specimens ER 1.470, ER 1.813 and OH
24 seem to be approaching the allometric level of the correlation g-op/pr-ba that concern to
H erectus/H sapiens but, in any case, out of the allometric level of Australopithecus. The evidence
of the fossil record is still very limited, but it suggests a change in the allometric relation between
the face length and the braincase length for the transition Australopithecus- early Horno. Hemmer's
(1969) observations are compatible with a process of neoteny, and we believe that the change in the
ancestral allometric relation for the brain and facial growth may indicate the beginning of this
process about 2.0 Myr ago.
Dommergues el al (1986) use the term «hypermorphose néoténique» to define the course of
(2) Human ontogeny ought not be considered as a discrete sequence of several growth phases, but a continuous process
characterized by total or partial changes in growth and development rates through the ontogeny, that produces characteristic
growth alIometries (see Alberch, 1985).

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human evolution. arguing that this evolution was characterized by both a decrease in the rate of
development and a delay in sexual maturation. Alternatively. we can consider human evolution as
the result of a process of neoteny and a delay in the offset signal for growth. We think that in this
issue lies one of the main sources of confusion in the debate about human neoteny. We agree with
Shea (1989) that the prolongation of growth in time does not equal or require the dissociation and
retardation of the patteros of shape ehange. However. we are out of keeping with this author that a
process of neoteny does not imply a prolonged growth in time or delayed maturity. Shea (1989)
assumes that in a process of paedomorphosis via neoteny descendant adult size and duration of
growth remain unehanged. If we accept this eondition strietly. we can discard the process of
neoteny as a possible mechanism to explain human evolution. Accordingly. Shea (1989) concludes
that ~A careful analysis of human development. morphology. and Jife history panems reveals little
concordance with the predictions of neoteny based on aecepted eriteria (p. 97). However. Shea
(1989) writes: dn humans. we do extend in time the early period of rapid prenatal and early
post natal brain growth .... thus attaining a relatively juvenilized gross skull form with a large.
bulbous cranium.... 1 consider the relative size of the brain and neurocranium as evidenee of
neoteny (p. 82). We believe that a decrease in the rate of development may imply a delay in the

g-op

200 E

180

M • OH-5
+?
F
160
ER-1813 WHK-TDW.
.
ER-406
transposition of
brain case size

OH-24 +
140 WT-17000

+ Australopithecus
specimens

120 +?

80 100 120 140 160 mm

pr-ba

FIG. l.-Redrawn lrom the diagram presented by Hemmer (1969. lig. 2) lor the allomelry glabella-
Opislhion/proslhion-basion (g-op/pr-ba) in a modern population (auslralian aborigines; M: males. F: lemales), and
in some hominid lossil specimens. Thin lines represento according lo Hemmer. the limits 01 the range 01 variatíon
01 modern sapiens. We have added data (taken on casts) lor the lollowing specimens: ER-147O, ER·18J3. ER-406;
OH-24. OH-5. WR-17000. and WHK TDW (reconstruction 01 A. afarensis). B: Broken Hil!; E: H. erectus;
N: Neanderta1s; S: Steinheim

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58 JOSE MARIA BERMUDEZ DE CASTRO Y MANUEL DOMINGUEZ-RODRIGO

offset signal for growth (and this is an hypothesis to be tested) producing adults larger than the
adult of the ancestral species, but not necessarily peramorphic (Fig. 2). We cannot be limited by the
rules of precise definitions of heterochrony, but we must consider that heterochrony is a potentially
heuristic methodology to understand morphological evolution. A static conception of ontogeny
might leads to problems such as those presented here (see Alberch, 1985). Furthermore, we think
that the study of particular anatomical features cannot be used to reject the role of neoteny in
changes characterizing the evolution of the genus Hamo (Lieberman, 1984; Dean & Wood, 1984;
Bromage, 1986).
Bromage (1986) considers that «The concept (of neoteny) is unsatisfactory to explain thc multi-
factorial changes accompanying the evolution of complex anatomical systems». We believe that
Bromage's (1986) observations on the similarities between the craniofacial remodeling patterns in
Australopíthecus and early Homo are compatible with a mode! of neoteny; this process only implies
a change in the rate of deve!opment, but not a change in the development or growth patterns.
However, we do not defend that the evolution of the genus Horno can be explained as a pure case
of neoteny with a delay of the offset signal for growth; but we believe that the increase in the
ontogeny time period was the main process characterizing human evolution, and that this process
was produced by a decrease in the rate of development. Other heterochronic processes affecting
the whole organism or particular anatomical regions could have influenced the evolution of the
genus Horno. For instance, the fossil record suggests that sorne increase of the overall growth rate
may be responsible for the presence of certain traits, which have been considered as synapomorphies
in all Middle Pleistocene hominid groups. The thickened tabular bone in the cranium and thickened
cortical bone in the postcranium (see Kennedy, 1985), as well as the considerable amount of dentine
deposition in the anterior teeth, which characterizes all specimens usually attributed to H erectus
reflect, in our opinion, a certain increase of the overall growth rate in these hominids. The

A
al

Shape

a
Time

FIG. 2.-Ontogenetic trajectories 01 Homo sapicns (D) and his ancestral species (A). A negative perturbation in the
rate of development 01 A produces a ehange in the ontogenetie trajeetory, and results in a paedomorphie
deseendant by a process of neoteny. This delay do not neeessan'ly implies that the deseendant species traseend
the ancestral shape, and were peramorphic in relation to A (which depends on the value 01 aK). However, our
model implies that the adults 01 the direct ancestors of rnodern humans were located in sorne place along the
line AD. a: onset age 01 growth; p: offset signal lor growth; K: shape growth rate during the growth periad. Based
on the rnodel 01 Alberch el al. (1979).

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superposlllon of this growth rate increase to the changcs in the lime period of the ancestral
allometries may explain the presence in H. ereclus of sorne fcaturcs which, we believe, are difficult
to undcrstand in adaptive terms, though other ones may arise as anatomical solutions to biomecha-
nical problems (see Smith, 1983). Though the discussion of this problem is outside the limits of this
work, we suggest however that these insights may constitute a potentially useful methodology to
focus future studies of hominid variability and evolution.

INFERENCES PROM THE ARCHAEOLOGICAL RECORD

Behaviour -an ecological factor of vital importance for the understanding of evolution, as the
intercessor among the individual, the community and the environment- is a perfect measurer not
only of the degree of adequacy of the different kind of species, but also of the index of their
behavioural development, which can be observed largely in the extent of their operativity in the
processing of information. This ability, so much more complex as the species is evolved, from a
neurophysiological consideration, is responsible for the degree of social interaction within groups,
only conditioned by the proximity and tolerance among the individuals that form part of them and
the use they make of territory.
It would be right to state that a species's behaviour is therefore ümited by the extent of its
evolutive development -which grants a greater degree of possibilist reaction as the magnitud e of
the instinctive conduct decreases- and by the conditionalities set forth by the environmental
parameters. Bearing in mind' that behaviour is a crucial factor in the global interpretation of
evolution -which the traditional paradigm has hardly considered- it becomes necessary to value it
adequately by using such criteria. Thus, since we are interested in the causes of somatic changes,
then we should al so focus our attention on behavioural alterations which, though in sorne instances
could be easily explained in terms of adaptative readjustments due lo a modification of the
parameters that rule the selective pressure, in other cases its exegesis should be worked out in the
same terms as the phenotype alterations. Considered in this way, it could be appropiate to talk
about behaviour evolution, whose comprehension should be made through a «phylogenetic» inter-
pretation of behaviour itself in a liule scale. That is to say, a conduct change is only possible from a
previous pattern whose alteration makes feasible the appearance of a new way of reaction, that
derives, strictly speaking, from the anterior formo This criterion, implicit in most of the ethological
research, has helped to create comparative models that have permitted to observe the existent
variability in order to evaluate it properly.
At sorne time before two million years ago a new kind of behaviour appe,!rs in the hominids's
realm, coinciding with the oldest archaeological record, whose general characteristics differ-in sorne
aspects in a radical way- from the basic behavioural pattern of the primate ambit. After nearly two
decades of testing the Plio-Pleistocene living floors of East Africa to evaluate their degree of·
integrity and resolution, a con sen sus was reached about the dynamics of the formation of such
artefact-plus-bone concentrations, aUributing their main authorship to hominids. This behaviour,
apart from the social implications that can be inferred, may be set up according to the next
evidences:

1. The archaeological sites appeared as a result of the reiterated accumulation of carcasses that
were transported from the points where they were obtained to central reference places -with
recurrent dispersal and reunion of the group at this chosen localities- to consume the meat they
contained (Bunn, 1981, 1982, 1983; Bunn & Kroll, 1986; Isaac, 1983a, 1983b, 1984; and PoUs, 1983,
1984, 1988). This means a series of innovations with regard to the general lines of the previous
subsistence behaviour:

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A. Meat eating in significant quantities; at least in an average substantially greater than the rest
of living primates.
B. Postponement of food consumption.
C. Transport of food and communal consumption at a central place.
D. A greater capability of tenitorial structuration. that would have in volved an extensive degree
of forethought and planning and/or strategic anticipation.

2. The presence of Iithic tools and stone debris in the sites can be accounted for its employment
in the processing of carcasses. which permited to have access to as wide a taxonomic variety as the
archaeological record demonstrates (Bunn. t 981; Potts & Shipman. t 98 t; Toth. 1982). However. this
fact reveals a series of abilities unknown in extant apes:
A. The capability of elaborating operative chains, that get further than the mere metabiologic
usage of certain vegetable and lithic items by sorne superior primates.
B. Valoration of the raw materials in the manufacture of artifacts to the extreme of transporting
it a10ng several kilometers.
This new behaviour, defined through the central-place foraging hypothesis (Isaac, 1983) is due, in
its whole consideration, to an increase in the sociability of the hominid groups responsible for the
living floors and in their capability of processing the information received from the environment.
Nevertheless, what was the real cause of this behaviour? At first sight, it might be thought that a
change in the ecosystem was the instigator of the whole process. The available data indicate a
c1imatic alteration at the end of the Pliocene, which consisted of a decrease of the humidity index
that would have provoked a new configuration of the east african flora and fauna (Bonnefille, 1976;
Hanis, 1983; VVAA, 1985). However, even with such readjustments, the Plio-Pleistocene savannah
was somewhat moister than it is today. It is therefore very likely that the bush areas occupied a
larger land extension than they do in the modern ecosystem. But even so, the alteration suffered by
the environment almost 2.5 million years ago was tremendously important because it helped to
reduce the habitats of several species, to promote new adaptative trends (specially in perissodactyla)
and because it offered a new space to newly developed strategies. This is just what seems to happen
to the hominids: whereas the australopithecines had to adapt themselves to a more reduced habitat,
the primigenial members of our genus knew how to enlarge their ecological niche to avail of the
resources offered by the open plains.
However, the behaviour inferred from the archaeological record does not seem to respond to a
simple adaptation to the new conditions issued in the environment. The general behavioural pattem
necessary for the anthropic accumulations need, as much as a new way of adaptation, a series of
abilities and operative capabilities, only adquired through an intemal process, that exceed those
observed in extant apes. Thus, this behaviour is not due to a mere adaptative readjustment, always
comprehensibIe within a strictly ethologicaI frame, but to a new adaptation issued from an impro-
vement of the capability to process information, which would be itself related to a redefinition of
the social tieso The lack of this eIement would have prevented a conduct of this kind from having
appeared beforehand.
Earlier we have interpreted the somatic changes that emerge with Horno from a heterochronic
consideration of neoteny. Now we mean to assess that such a process is also the reason of the
behaviour responsible for determined anthropic accumulations. If these are due to the establishment
of central places where food is transported and presumably shared, in a cooperative attitude, it may
be asked what kind of social and biological changes caused such reaction.
Conceming the first type of alteration, it should be stated that a society becomes more cooperative
as the pressure from the exterior is greater. This can be observed in the primates that inhabit a
forest ecosystem and those who live in the savannah. In the Iatter, the vegetable resources are
scarcer and more scattered and the competition for them is stronger. Before such circumstances,
the usual action is an increase in the variety of the products consumed by adopting a diet that

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tends to become omnivorous. As the savannah is more hostile than the forest, due to the existent
pressure on resources and the number of predators that occupy an ecological niche in that
ecosystem, the way that primates behave is using an adaptative strategy of reinforcement of the
social links, together with a development of the agression instinct. However, even though such
modifications have been carried out, the social structures that lie beneath are still the same, with
the maintenance of the hierarchies and the reproductive and subsistential strategies that are
common to the rest of primates.
The conclusion that can be drawn from the observation of the archaeological record, nevertheless,
is that the general behavioural pattern of subsistence is abandoned in favour of a more planned
conduct, that must have emerged in more cooperative societies, as a result of further increasing the
reinforcement of the internal links. But, what promoted such change in the social relationships? One
could argue about the possibility that sorne hominids simply became more intelligent. However, the
increase of intelligence means a raising of the degree of potentiality on the environmental operativity
that does not necessarily imply a readjustment of the subsistence strategies. That is, the improvement
of the way of processing information would have reported a greater capability of acceding to a
wide spectrum of resources -among which meat would be an important element-, but the way of
consumption should not be altered. It could only be expected a slight postponement of meat
ingestion beca use of the displacement of the carcasses obtained to other places, in order to be safe
from the open-plain predators. But if this had been realized according to the primate behavioural
pattern, the displacement of meat pieces would ha ve been comparable to the action of determined
carnivores, which does not propiciate the formation of the bone concentrations that we observe in
the archaeological record, beca use it always depends on the place that carcass is obtained. The
archaeological bone accumulations, however, seem to indicate the establishment of referential
places previously to the meat obtainment. Thus, the postponement of food consumption could be
attributed not only to avoid the hostility of the open areas, but mainly to bring a part of it (or the
whole of it) to the rest of the group (Fig. 3). This fact together with the hypothesis that in this kind
of action only a fraction of the group would have participated (What could have been the role of
the females with offspring in the obtainment of carcasses?), concedes a greater consisten ce to the
interpretation that this behaviour is due to as much a necessity of increasing the internal cohesion
as to the adquisition of a better intelectual capability, because both factors are intimately related. If
this assumption is not discussed, then the next step will be the discernment of the reasons of such a
social reinforcement. If this one was favoured by the raising of intelligence, on an environmental
stage with well-defined criteria, it is logical to think that the initial change was a biological one.
Previously, from an heterochronic perspective, we have argued that the physical traits that
appear with our genus might be explained by one of the next possibilities: rate hypermorphosis or
neoteny. If we consider the first of them, the neonates would have been taller than their predecessors
and perhaps their morphological pattern could have been slightly altered. But a change due to rate
hypermorphosis would not create a helpless offspring that needed more attention and a longer
period of living together with their progenitors. So, if early Horno had experienced this sort of
change, keeping the same development pattern as their predecessors, the social relationships within
the group should not be altered significantly. A neotenical process, however, would have imposed a
change in the nature of this relationships, beca use of the prolongation of the development period,
increasing, therefore, the lenght of the infantile and juvenile stages and making the progeny at the
same time more defenseless ' and needy of paternal careo This fact could have caused the need of a
tighter social cohesion to take care of the offspring, this being the key to the alteration of the
relationships among the individuals of the group and giving rise to a cooperative behaviour, which
is the one inferred from the archaeological record.
The neotenic argument proposed to account for the origin of our genus is not new. Several
authors have used it for the same purpose (Washburn, 1967; Lorenz, 1971). Nevertheless, few of

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th em have investigated further into its causes a nd its close relation to th e behaviour that appears in
the end of the Pliocene. Isaac (1983) interpreted it in a convincing way, according to what he called
«culture-brain system», w hich consisted of treating brain and c ulture as co-evolutive elem ents that
were likely to have evo lved as a single adaptative compl ex: Culture appears because brain evolves,
but also beca use «enlarged brains require prolo nged infant dependency and high-quality nutrition»
clearly alluding to a process of neoteny and a dietary improvement.

F IG. 3.-The formalion of Ihe archaeological record respo nds /0 planned ac/ions, w h ere /h e hominids in volved
wou ld ha ve es /ablish ed relerence places or common operalive poin/s, nOI necessarily iden/i/ied wilh home bases,
previously lo /h e lransport 01 m ea/ resources. 1I /h ese hominids had kep/ /he basic s ubs is /en/ial primale pallern,
Ihe processing 01 carcasses wou ld have been carried out in s i/u (A), w here Ihe carcass was oblained . or in a
nearby s hel/ered place (B), a/ways condilioned by Ihe exacI poin/ 01 Ihe oblainmenl 01 /h e carcass ilself. Howe ver,
Ih e prelerence for areas 01 dense vegela/ion close la rivers Clnd lakes (C), as Ihe siles mighl indica/e COL/ld be due
lo Ihe exislence o/ CI wider speclrum o/ lilhic resources Ihan in /h e open-plain areas (A, B), and beca use th e
n ~l mber o/ preda/OI-s is more reduced. BU! Ih is being Ih e on ly reason, Ihere wou ld nol ex is l any oppor/unily /or
bone accL/mulalions, as Ihe carcasses could have been Iransponed lo any place indislÍn clly (C). Never/h eless,
IhoL/gh lhis accL/mu la/ion could have happen ed, dL/e lo Ih e ha zardous inciden ce 01 Ihe hominids on /he same
Sp01S, dL/ring a lapse 01 lime Ihal mighl span an L/nlimiled period, il wou ld nol have bee n res /ricled lo so a
redL/ced area as Ih e arclweological s i/es are.
Therefore, bearing in mind lhese cons ideralions and Ih e presence ol/oreign ra w malerial in a vas/ number 01
s i/es (which conlradicls Ihe idea lha/ si/es were brief episodes in /h e subs is/ence behaviour), iI migh l be
concluded lhal Ihese artefa c/-plus -bone concenlralions were cenlral-re/eren ce places crea/ed under new social
and biological circumSlan ces.

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Basically, the retardation of development obscrved in Horno is just the continuation of the
general trend to its prolongation in extant apes, which increases itself according to their degree of
evolutive complexity (Shultz, 1956). Furthermore, between the genus Horno and the living anthropoids
there exists an authentic variation in the time parameters of each of the development phases (a
circumstance that is accompanied by opposed subsistence strategies), which gives further support
to the hypothesis that the intermediate links between both extremes must be found in the fossil
record.
But if the retardation of such process results quantitatively more important as the evolutive
scale gets more complex and its apparition in Horno is perfectly comprehensible following these
criteria, why were the consequences so drastic? The well-defined trend to the prolongation of the
infantile and juvenile periods has deeply influenced primate behaviour. The c10se dependency of
youth gives them the possibility of learning adults's reactions. If this is still prolonged then it may be
observed a raise of adquired behaviour in detriment to inborn conduct. This leads to the conclusion
that the longer the parental dependency is, the greater the range of behavioural options become
-helped by a better understanding of the information- which turn those who are involved in it
into more intelligent beings. However, an increasing retardation of development means a postpone-
ment of the addition of new generations, which is vital for the survival of the species limited to only
one new individual per enlightment. This trend of a .K» reproductive strategy is as much pronounced
as the degree of complexity of primate evolution becomes greater. Whereas in prosimü multiple
enlightment is still common, in the great apes there is a reduction of it and the normal rule is one
descendent per parturition. But the really important factor is that the more evolved a primate is, the
longer the length of time is between one enlightment and the next; thus becoming the «K» strategy
more extreme. But if this is carried out to a determined limit-where certain threshold is trespassed
-it supposes a great risk for the species, which is set on the verge of extinction if any kind of
selective readjustment occurs (Lovejoy, 1981). This is probably the reason that the differences in the
duration of gestation and spacement of successive descendents among anthropoids are rather
unimportant; even though sorne of them are superior to the others in evolutive terms. This fact is
due to their being just in the limit of the «1(» strategy, where any attempt to get further could be
prejudicial.
In order to prolong the development period and to enjoy its consequences, it would be necessary
to alter the basic subsistential pattem and, therefore, the social structure, as Lovejoy (1981)
correctly states, tuming from a hierarchical organisation to a cooperative one, and looking after the
offspring in a proper way, with all that this represents in the alteration of feeding behaviour.
Nevertheless, we do not agree with Lovejoy's hypothesis as to the moment of appearance of this
modification, changing it from the genesis of bipedism, as he states, to the origin of Horno. One of
the reasons that impel us to do so is not only that the first somatic indications of such process
appear with our genus, but also that a behavioural change of such a magnitud e needs an operative
capability that superior primates -and possibly first hominids too- lacked. And the most ancient
evidence of this ability is demonstrated by the appearance of the archaeological record which, in
turn, coincides with a relevant brain enlargement in Horno with regard to the australopithecines,
being the craneal capacities, in sorne cases, the double.
This authentic increase of intelligence would have caused a wider operative ability in the
exchange of information, creating a more complex capability of reaction towards the environment
and the society. The development of attitudes of reciprocity within the group would have led to a
greater cooperation, and the processing of information with more efficiency would have augmented
the operativity on the environment by making it more intelligible. This could have favoured the
formation of central places, like those that appear on the record, increasing the efficacy of moving
through diverse habitats, and creating a new ecological niche not constrained exclusively to a
concrete kind of habitat.
They would have developed also the capability of estimating the raw material and of linking
operative chains capable of transforming it inta lithic industry, with which access to a diversity of

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meat resources could be gained, and which was also probably used to elaborate other sorts of
instruments. The basic subsistence primate pattem that demands the inmediate satisfaction of
instinct is abandoned as the first traces of a conduct that responds to the planning of actions that
go beyond the former appears.
This amplification of the environment comprehension could be a logical consequence of the
retardation of development, which would have meant not only a quantitative increase of the
dependency pe riod , but also a qualitative augmentation of it. That is to say, the neonate could have
had more time to leam and more capacity to do it. The prolongation of parental care would have
been responsible of the transmission of information to the progeny, which would get in this way all
the knowledge needed for survival. This means at first a longer maternal dependency -it is likely
that males participated in this phase too- in the infantile stage, where the attentions received
would have prepared the offspring, psycologically, for the development of their faculties. During the
juvenile phase the progeny would have enlarged their contact area, from the family group to the
social group, leaming from the adults the behaviour that would be indispensable to subsistence and
to strengthening the group's organization. This would have reduced the inbom conduct to its basic
expression in favour of the adquired knowledge, potentially more useful.
• However, we have seen how this trend to the «I<>t extreme has sorne important consequences for
the members of the group, who must adopt a subsistence strategy whose basic lines differ from
those of the rest of primates. It has always been said that the main reason for the change could
have been the care of a defenceless offspring. If this had been the only motif, the species could
have risked extinction beca use with the prolongation of the development period the lapse of time
between successive enlightments would have been greater. Thus, if the degree of intelligence is
increased and the social links are redefined, there is, in tum, a retardment in the generational
renovation, which is risky for a species whose new ecological niche ineludes dangerous habitats,
and that needs to be more prolific than their evolutive congenerers -who preferred the sheltered
areas- to compensate the los s of individuals. The success, of the new behaviour, therefore, could
be accounted for by the next reason: The prolongement of development could not have needed to
alter the length of time from a parturition to the next one, if the augmented progeny was properly
looked after. So, just by keeping the anthropoid birth parameters and by enlarging development at
the same time -with an increased parental dependency- the social reorganization would be then
more intelligible, because cooperation would have become necessary not as much to care for the
defenceless offspring, but for the inereasing number, so that the infant would have needed, therefore,
the participation of all the members of the group for their survival.
This hypothesis could be corroborated by the character of diet itself. Sorne authors assess that
to develop and keep a brain like Horno habilis s brain, it is essential for diet to be rich in energetic
terms (Martin in Lewin, 1982). Isaac (1983), in his «brain-culture» system, states that a dimensional
change in brain requires an alteration of the index of calories and proteins of the food consumed,
being necessary a high-quality nutrition only possible if eating meat resources. Thus, the significant
meat consumption, whose vestige is elear in the archaeological record, made these innovations
feasible.
One of the further consequences that this change of diet could have meant is that it might have
made females more prolific, predisposing them to be more fertile (Darwin, 1871).
When talking of the passage of a hierarchical society to a cooperative one, with males engaged
in breeding, it is commonly assumed the formation of stable couples or familiar nuelei (Lovejoy,
1981). H males had to participate in this task, it is logical to suppose that they were integrated in a
social system that resulted, essentially, almost utterly human. To argue the motivations of this
relationship it has been proposed the reciprocal interaction argument, where both, male and Jemale,
could have been beneficiary of the new system. Lovejoy's hypothesis is particularIy shocking in this
regard, as it pretends that males would have accepted such an association in return of permanent
sexual relationships -disentangled froro estrus-, whose origin must be sought in a slow replacement
of the instinctive attraction by another of epigamic character. But this, in our opinion, results

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extremely premature as the epigamic attraction is the result of a psicophysiological organization

only observable in modern mano Placing its origins at the beginning of the Pliocene, as Lovejoy
does, would mean accepting that the capability of abstraction existed in such a remote time, where
there is no evidence thereof.
As a matter of fact, males could simply have consented to cooperate with fe males without
needing to get from them a sexual satisfaction of that kind. Cooperation could basically have been
carried out by means of a survival strategy, as it happens among hilobatids, in which there is a c1ear
precedent. The formation of stable couples, however, is not indispensable to maintaining a system
like the one proposed. Males could have feh obliged -by a mere necessily of adaptation to the
environment- to participate in the custody of lhe progeny, not unly in a defensive way as the rest
of primates do, but getting the meat necessary for an improvemenl of diet, too. They would have
cooperated in the social distension, making it possible for the offspring to enjoy the didactic
potential of a relationship of this kind.
If this had been the case, it might be expected a relevant dimensional variability due to the
sexual dimorphism existent in a system with these features. In this respect, the observations of the
size and shape variability that has been found in Horno habilis (see Chamberlain, 1999) have led
sorne authors (eg. Groves & Mazak, 1975; Stringer, 1986 y Liebermann el al, 1988) to conclude that
more than one species are represented in the early Horno hypodigm or that sexual dimorphism
could explain this observed variation (White el al, 1989 y Tobias, 1985). However, other authors
state that the fossil remains do not seem to offer a solid basis to support any of the options
(Harcourt el al, 1981; Martin & May, 1981).
Thus, with the appearance of families or with the maintenance of a poligamic society of
cooperative males, the retardation of development together with an ostensible increase of intelligence
would have benefitted the shift to a more solidary behaviour that, in turn, would have propitiated a
longer parental dependency and a greater capability of informative operativity.
Bearing in mind the quantitative improvement of diet, this could have had demographic conse-
quences that, together with a social system of reciprocity, would have set the basis for the
expansion of our genus, which would reach its height with the abandonment of the African
continent and the extinction of the rest of the hominids.

CONCLUDING REMARKS

Heterochrony is a useful way to study evolutionary changes in human evolution. In this respect,
we consider that the concept of neoteny has a lot to offer to understand the first stages of human
evolution (contra Bromage, 1986), and that it is not a bankrupt concept lo explain sorne aspects of
our development (contra Shea, 1989). Modern humans are not differentiated from living great apes,
and probably from Australopilhecus simply by a prolongation of the growth period (or by a delay of
the offset signal for growth). This is a peramorphic process that would have happened via time.
hypermorphosis (= hypermorphosis). Instead, we are characterized by an extension of all our life
history periods in relation to the great living apes. To our ,knowledge, no heterochronic process
defined up to date, except neoteny, fit this human feature; we need either to propose a new
peramorphic process of heterochrony in which the rate of development and, therefore, the ancestral
allometries remain unchanged, but there is an extension of the entire growth period, or simply to
accept that this extension was produced via neoteny by a decrease in the rate of development. The
pattern of brain growth in modern human s (see Martin, 1983) advocates for a such decrease,
though further experimental research on heterochronic processes would be necessary to answer
these questions. In any case, we believe that the beginning of the extension of the different growth
periods was probably related to the speciation that supposed the appearance of the genus Horno.
This would help to explain the appearance of the archaeological record, which is better understood
from a view of social reorganization due to a biological change in the operative and interactive

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capabilities and to an alteration of breeding behaviour, that would have caused the necessity of
becoming a more cooperative society.
We are firmly persuaded, however, that a simple process of neoteny cannot account for all the
evolutionary changes characterizing our lineage. We think, for instance, that the presence of certain
synapomorphies (long bone shaft thickness, thick bone of the cranial walls and mandibular bone, or
a considerable deposition of dentine in the incisors) in those Middle Pleistocene hominids which
have been generally attributed to H ereclus, or considered as «archaic» H sapiens (see Wolpoff,
1980) may be explained by an increase of the overall growth rateo If this is true, the so-called
multiregional model to explain the origin of anatomically modern human populations (see for
instance Wolpoff el al, 1984; Wolpoff, 1989 or Kramer, 1991) ought to assume that the evolution of
diverse populations in different parts of the world was characterized by a new decrease of the
growth rate to get the gracilization that is common in all modern human populations. But, how is it
possible to justify such a parallel evolution? In contrast, the acceptance of the single origin or
replacement model (see for instance Howells, 1976 or Stringer & Andrews, 1988) might imply the
hypothetical existence of an African Horno population which did not experience an increase of the
overall growth rate similar to that of H erectus. This hypothetical population would have not shared
with H. erectus those derived features that arose from the increase of growth rateo Therefore, those
features that define the gracile skeleton of living humans would be plesiomorphous, and not
derived ones, as suggested by Stringer & Andrews (1988). These insights have important phylogenetic
and taxonomic implications, and merit further research and discussion from a cladistic and hete-
rochronic view (see Fink, 1982).

ACKNOWLEDGEMENTS

This research has been supported by the DIGICYT projects PB88-0l20 and PB90-0l26-C03-01.

BIBLIOGRAFIA

AIELLO, L. & DEAN, CH. (1990): An lnlroduclion lo Human Evolutionary Analomy. Academic Press. London.
ALBERCH, P. (1985): «Problems with the interpretation of development sequences». Syslemalic Zoology, 34: 46-58.
ALBERCH, P.; GOULD, S. J.; OSTER, G. F. & WAKE, D. B. (1979): «Size and shape in ontogeny and phylogeny».
Paleobiology, 5: 296-317.
BEYNON, A. D. & DEAN, M. C. (1988): «Distinct dental development patterns in early fossil hominids». Nature, 335:
509-514.
BEYNON, A. D. & WOOD, B. A. (1987): «Patterns and rates of enamel growth in the molar teeth of early hominids».
Nature, 326: 493-496.
BINFORD, L. (1981): Bones, Ancienl Men and Modern Myths. Academic Press. New York.
BOLK, L. (1926): Das Problem der Menschwerdung. Gustav Fischer. Jena.
BONNEFILLE, R. (1976): «Palynological evidence for an important change in the vegetation of the Omo basin
between 2,5 and 2 million years ago». In C. Howell, R. Leakey, G. Isaac & Y. Coppens (eds.): Earliesl Man and
lhe Environments in the Lake Rudolf Basin: Stratigraphy, Paleoecology and Evolulion. The University Chicago
Press. Chicago: 421-431.
BRACE, C. L. (1962): «Cultural factors in the evolution of the human dentitioO). In M. F. A. Montagu (ed.): Cullure
and the Evo/ution of Man. Oxford Vniversity Press. New York: 343-354.
BROMAGE, T. G. (1986): A Comparalive Scanning Eleclron Microscope Sludy of Facial Growth and Remodeling in
Early Hominids. Ph. D. Thesis. University of Toronto. Canada.
- (1987): «The biological and chronological maturation of early hominids». Journal of Human Evo/ution, 16:
257-272.
BROMAGE, T. G. & DEAN, M. C. (1985): «Re-evaluation of the age at death of inmature fossil hominids». Nature,
317: 525-527.
BROOM, R. & ROBINSON, J. T. (1951): «Eruption of the permanent teeth in South Africa fossil ape-meo». Nalure,
167: 167-443.

T. P., 1992, nI! 49

(c) Consejo Superior de Investigaciones Científicas http://tp.revistas.csic.es

Licencia Creative Commons 3.0 España (by-nc)
 HETEROCHRONY ANO THE PALEOANTHROPOLOGICAL RECORD: THE ORIGINS OF THE... 67

BROWN, F.; HARRIS, J.; LEAKEY, R. & WALKER, A. (1985): «Early HO/r/o erectus skeleton from west Lake Turkana,
Kenya». Nature, 316: 788-792.
BUNN, H. (1981): «Archaeological evidence for meat-eating by Plio-Pleistocene hominids from Koobi-Fora and
Olduvai Gorge». Nature, 291: 574-577.
(1982): «Meat-eating and Human Evolution: Studics on the Diet and Subsistence Patterns of Plio-Pleistocene
Hominids in East Africa» . Ph. D. dissertation, University of California, Berkcley.
(1983): «Evidence on the diet and subsistence patterns of Plio-Pleistocene hominds at Koobi Fora, Kenya,
and Olduvai Gorge, Tanzania». In J. Clutton-Brock & C. Grigson (eds.): Animal~ und Archaeology: Hunters
and their Prey. B.A.R. International Series. Oxford: 21-30.
BUNN, H, & KROLL, E. (1986): «Systematic Butchery by Plio-Pleistocene Hominids at Olduvai Gorge, Tanzania» .
Current Anthropology, 27: 431-452.
CONROY, G, C. & VANNIER, M, W, (1987): «Dental development of the Taung skull from computerized tomography» .
Nature, 329: 625-627.
DARWIN, C. (1871): The Descent 01 Man. Modem Library. New York.
DAY, M. H. & LEAKEY, R. E. F. (1973): «Ncw evidence of the Genus Homo from East Rudolf, Kenya J¡¡ , American
Journal 01 Physical Anthropology, 39: 341-354.
DAY, M. H.; LEAKEY, R. E, F, & WALKER, A, C. (1976): «New hominids from East Turkana, Kenya». American
Journalo{ Physical Anthropology, 45: 369-436.
DAHLBERG, A. A. (1963): «Dental evolution and Culture». Human Biology, 35: 237-249.
DEAN, M. C. (1987): «The dental deve/opment status of six East African juvenile fossil hominids». Journal o{
Human Evolution, 16: 197-213.
BEER, DE G, R. (1930): Embriology and Evolution. Clarendon Press, Oxford.
- (1948): «Embriology and the evolution of Mam), In A. du Toit (ed.): Robert Broom Commemorative Volume.
Special Publications o{ the Royal Society o{ South Alrica: 181-190.
DEMIRJIAN, A. (1978): «Dentitiom). In L. Falkner & J, M. Tanner (eds.): Human Growth. 2, Plenum Press. New York:
413-444,
DOMMERGUES, J. L.; DAVID, B. & MARCHAND, D. (1986): «Les re/ations ontogenése-phylogenése: applications paléon-
tologiques». Geobios, 19: 335-356,
FINK, W. L. (1982): «The conceptual relationship betwecn ontogeny and phylogeny» , Paleobiology, 8: 254-264,
GOULD, S. J, (1977): Ontogeny and Phylogeny. Harvard University Prcss. Cambridge,
GRINE, F. E. (1987): «On the eruption pattern of the permanent incisors and first permanent molars in Paranthro-
PUSl). American Journal o{ Physical Anthrupology, 72: 353-359,
- (1989): «New hominid fossils from Swartkrans Formation (1979-1986 excavations): craniodental spccimens» .
American Journal o{ Physical Anthropology, 79: 409-449.
HARCOURT, A. H.; HARVEY, p, H.; LARSEN, S. L. & SHAT, R. V. (1981): «Testing weight and brecding systems in
primates», Nature, 293: 55-57.
HARRIS, J. M. (1983): «The fossil ungulates: Proboscidea, Perissodactyla and Suidae». Koobi Fora Research Project
2, Clarendon Press. Oxford,
HEMMER, H. (1967): «Der phylogenetische gestaltwandel des hominidenscha:dels in allometrischer betrachtung»,
Homo-9. Tagung der Deutschen Gesellschalt lür Anthropologie: 139-143.
- (1969): «A new view of the evolution of Mam. Current Anthropology, 10: 179-180.
HOWELLS, W. W. (1976): «Explaining modern Man: evolucionists versus migrationists». Journal 01 Human Evolution,
5: 447-495.
ISAAC, G. (1983 a): «Aspects of human evolution», In J. M. Harris (ed.): Essays on Evolution: a Darwin Centenary
Volume, Cambridge University Press. Cambridge: 32-58.
(1983b): «Bones in contention: competing explanations for the juxtaposition of Early Pleistocene artifacts and
faunal remains». In J. Clutton-Brock & C. Grigson (eds.): Animal and Archaeology: and Archaeology: Hunters
and their Prey. B.A.R. Interoational Series. Oxford: 3-19.
(1984): «The archaeology of human origins: studies of the Lower Pleistocene in East Africa». In F. Wendorf
& A. Close (eds.): Advances in Old World Archaeology, 3, Academic Press. New York: 1-87,
JOHANSON, O, C. & WHITE, T. D. (1979): «A systematic assessment of early African hominids», Scie n ce, 203: 321-
330.
KEITH, A. (1949): «Foetalization as a factor in human evolution». In A new Theory o{ Human Evolution. Watts.
London: 192-201.
KENNEDY, G. E. (1985): «Bone thickness in Homo erectuSl), Journal of Human Evolution, 14: 699-708.
KRAMER, A. (1991): «Modero human origins in Australasia: Replacement or evolution», American Journal of
Physical Anthropology, 86: 455-473,
KROGMAN, W, H. (1972): Child Growth. University Michigan Press, Ann Arbor.
LEAKEY, R. E. F. & WOOD, B. A, (1973): «New evidence of the Genus Homo from East Rudolf, Kenya». American
Journal 01 Physical Anthropology, 39: 355-368.
(1974): «New evidence of the Genus Homo from East Rudolf, Kenya». American Journal of Physical Anthro-
pology, 41: 237-244.

T. P., 1992, nO 49

(c) Consejo Superior de Investigaciones Científicas http://tp.revistas.csic.es

Licencia Creative Commons 3.0 España (by-nc)
 68 JOSE MARIA BJr:RMUDEZ DE CASTRO v MANUEL DOMINGUEZ-RODRIGO

LEAKEY, R. E. F. & WALKER, A. C. (1985): .Further hominids from thc Plio-Plcistoccnc of Koobi Fora, Kcnya ...
American Jouma/ of Physica/ Anlhropvlugy, 67: 135-163.
- (1988): .New Austra/opithecus boiseispecimens from East and West Lake Turkana, Kcnya ... American
lournal of Physical A nthropology, 76: 1-24.
LEWIN, R. (1982): «How did humans cvolve big brains?... Science, 216: 840-841 .
LoRENZ, K (1971): Studies in human and animal behavior. Harvard University Press. Cambridge, Mass.
LovFJOY, O. (1980): .Hominid origins: The role of bipedalism ... American Journa/ of Physical Anthropvlogy, 52:
250-262.
- (1981):. The origin of Man ... Science, 211: 341-350.
MANN, A. E. (1975): Paleudemographic Aspects 01 the South Alrican Australopithecines. University of Pcnnsylvania.
Philadelphia.
- (1988): .The nature of Taung dental Maturation ... Nalure, 333: 123.
MANN, A. E.; LAMPL, M. & MONGE, J. (1987): .. Maturational pattcrns in early hominids... Nature, 328: 673-674.
MANN, A. E.; MONGE, J. & LAMPL, M. (1990): .. Dental caution ... Nature, 348: 202.
MARTIN, R. D. (1983): -Human brain evolution in an ecological context». Fifty-Second James Arthur Lecture on
the Evolution of the Human Brain, 1982. American Museum of Natural History. New York.
MARrlN, R. & MAY, R_ (1981): .Outward signs of breeding... Nalure, 212: 339-342.
McNAMARA, K J. (1986): «A guide to the nomenclature of heterochrony•. Journal 01 Paleontology, 60: 4-13.
MONTAGU, M. F. A. (1962): «Time, morphology, and neoteny in the evolution of man. In M. F. A. Montagu (cd.):
Culture and the Evo/ution of Man, Oxford University Press. New York: 324-342.
P.ons, R_ (1982): «Lower Pleistocene site fonnation and hominid activities at Olduvai Gorge, Tanzania... Ph, D.
dissertation, University of Harvard, Cambridge, Massachusets.
(1983): «Foraging for faunal resources by early hominids at Olduvai Gorge, Tanzania». In J. Clutton-Brock
(ed.): Animals and Archae%gy: Hunters and their Prey. B.A.R. Intemational Series. Oxford: 51-62.
(1984): _Home bases and early hominids ••. American Scientist, 72: 330-347.
(1988): Early hominid activities at Olduvai. Aldine de Gruytcr. New York.
POTIs. R. & SHIPMAN. P. (1981): _Cutmarks made by stone tools on bones from Olduvai Gorge, Tanzania ••. Nature,
291 : 577-580.
ScHULTZ, A. H. (1956): «Postembryonic age changes... In H. Hofer, A. H. Schultz & D. Stark (eds.): «Primatologia•• 1.
Base! S. Karger. New York: 887-964.
SCHINDEWOLF, O. H. (1929): «Das problem der menschwerdung, ein palaontologischer ll}sungsversuch». lb. Preuss.
Geol Landesant., 49: 716-766.
SHEA, B. T. (1983): «Allometry and heterochrony in the African apes ... American lournal 01 Physical Anthropology,
62: 275-289.
- (1989): «Heterochrony in human evolution: The case of neoteny reconsidered». Yearbook 01 Physical Anthro-
p%gy, 32: 69-101.
SIMPSON, S. W.; LOVFJOY, C. D. & MEINDL, R. S. (1990): .Hominoid dental maturatiom. lournal 01 Human
Evolution, 19: 285-297.
SMITH, B. H. (1986): «Dental development in Australopithecus and early Homo+. Nature, 326: 327-330.
SMITH, F. H. (1983): «Behavioral interpretation of changes in craniofacial morphology across the archaic/modern
Homo sapiens transition... In E. Trinkaus (ed.): The Mousterian Legacy.· Human Biocultural Changes in the
Upper Pleistocene. BAR Intemational Series. Oxford, 164: 141-162.
STRINGER, C. B. & ANDREWS, P. (1988): «Genetic and fossil evidence for the origin of modem humans ••. Science,
239: 1.263-1.268.
TOTH, N. (1982): l<The stone technologies of early hominids at Koobi Fora, Kenya: an experimental approach». Ph,
D. dissertation, University of California. Berkeley. .
VVAA (1985): _L'environnement des Hominidés au Plio-Pleistocene». ColIoque InternationaL Foundation Singer-
Polignac, 1981. Masson.
WASHBURN, L. (1967): «Behaviour and the origin of man». Huxley Memorial Lecture, 1967. Proceedings 01 the
Royal Anthropologicallnstitute 01 Great Britain and Ireland' 21-27.
WOLPOFF, M. H. (1979): «The Krapina dental remains... American lournal 01 Physical Anthropology, 50: 67-114.
(1980): Paleoanthropology. Knopf. New York.
- (1989): «Multiregional evolution: The fossil altemative to Eden ... In P. A. Mellars and C. B. Stringer (eds.): The
Human Revolution: Behavioural and Biologica/ Perspectives on the Origins 01 Mudern Hu ma ns. Edinburgh
University Press. Edinburgh: 62-108.
WOLPOFF, M. H.; Wu XINZHI & THORNE, A. G. (1984): _Modem Homo sapiens origins: A general theory of hominid
evolution involving the fossil evidence from east Asia... In F. H. Smith & F. Spencer (eds.): The Origins 01
Mudern Humans.· A World Survey of the Fossil Evidence. Alan R. Liss. New York: 411-483.

T. P., 1992, nI! 49

(c) Consejo Superior de Investigaciones Científicas http://tp.revistas.csic.es

Licencia Creative Commons 3.0 España (by-nc)